Abstract
We manipulated dietary lead (Pb) levels of nestlings in wild populations of the great tit (Parus major L) to find out if environmentally relevant Pb levels would affect some physiological biomarkers (haematocrit [HT], fecal corticosterone metabolites [CORT], heat shock proteins [HSPs], erythrocyte delta-aminolevulinic acid dehydratase activity [ALAd]), growth (body mass, wing length), phenotype (plumage coloration) or survival of nestlings. The responses to three experimental manipulation (control, low and high: 0, 1 and 4 μg/g body mass/day) are compared with those in a P. major population breeding in the vicinity of a heavy metal source, a copper smelter. Our Pb supplementation was successful in raising the fecal concentrations to the levels found in polluted environments (high: 8.0 μg/g d.w.). Despite relatively high range of exposure levels we found only few effects on growth rates or physiology. The lack of blood ALAd inhibition suggests that the circulating Pb levels were generally below the toxic level despite that marked accumulation of Pb in femur (high: 27.8 μg/g d.w.) was observed. Instead, birds in the metal polluted environment around the smelter showed decreased growth rates, lower HT, higher CORT, less colorful plumage and lower survival probabilities than any of the Pb treated groups. These effects are likely related to decreased food quality/quantity for these insectivorous birds at the smelter site. In general, the responses of nestlings to metal exposure and/or associated resource limitation were not gender specific. One of the stress proteins (HSP60), however, was more strongly induced in Pb exposed males and further studies are needed to explore if this was due to higher accumulation of Pb or higher sensitivity of males. In all, our results emphasize the importance of secondary pollution effects (e.g. via food chain disruption) on reproductive output of birds.
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References
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693
Andersson S, Prager M (2006) Quantifying Colors. In: Hill GE, McGraw KJ (eds) Bird Coloration. Harvard University Press, Cambridge, pp 41–89
Baos R et al (2006) Adrenocortical response to stress and thyroid hormone status in free-living nestling white storks (Ciconia ciconia) exposed to heavy metal and arsenic contamination. Environ Health Perspect 114:1497–1501
Bauman JW, Liu J, Klaassen CD (1993) Production of metallothionein and heat-shock proteins in response to metals. Fundam Appl Toxicol 21:15–22
Belskii EA, Bezel VS, Lyakhov AG (1995a) Characteristics of the reproductive indices of birds nesting in tree hollows under conditions of technogenic pollution. Rus J Ecol 26:126–131
Belskii EA, Bezel VS, Polents EA (1995b) Early stages of the nesting period of hollow-nesting birds under conditions of industrial pollution. Rus J Ecol 26:38–43
Belskii EA, Lugas’kova NV, Karfidova AA (2005) Reproductive parameters of adult birds and morphophysiological characteristics of chicks in the pied flycatcher (Ficedula hypoleuca Pall.) in technogenically polluted habitats. Rus J Ecol 36:329–335
Berglund AMM, Nyholm NEI (2011) Slow improvements of metal exposure, health- and breeding conditions of pied flycatchers (Ficedula hypoleuca) after decreased industrial heavy metal emissions. Sci Total Environ 409:4326–4334
Berglund M et al (2000) Metal-bone interactions. Toxicol Lett 112:219–225
Berglund ÅMM et al (2010) Lead exposure and biological effects in pied flycatchers (Ficedula hypoleuca) before and after the closure of a lead mine in northern Sweden. Environ Pollut 158:1368–1375
Berglund ÅMM, Koivula MJ, Eeva T (2011) Species- and age-related variation in metal exposure and accumulation of two passerine bird species. Environ Pollut 159:2368–2374
Berglund ÅMM, Rainio M, Eeva T (2012) Decreased metal accumulation in passerines as a result of reduced emissions. Environ Toxicol Chem 31:1317–1323
Borowska J et al (2004) Heavy metal accumulation and its effects on development, survival and immuno-competent cells of the housefly Musca domestica from closed laboratory populations as model organism. Fresenius Environ Bull 13:1402–1409
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brzek P et al (2009) Developmental adjustments of house sparrow (Passer domesticus) nestlings to diet composition. J Exp Biol 212:1284–1293
Burger J (2007) A framework and methods for incorporating gender-related issues in wildlife risk assessment: gender-related differences in metal levels and other contaminants as a case study. Environ Res 104:153–162
Burger J, Gochfeld M (2000) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health B 3:59–78
Carere C et al (2003) Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm Behav 43:540–548
Custer TW, Franson JC, Pattee OH (1984) Tissue lead distribution and hematologic effects in American kestrels (Falco sparverius) fed biologically incorporated lead. J Wildl Dis 20:39–43
Dauwe T et al (2000) Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metal pollution? Arch Environ Contam Toxicol 39:541–546
Dauwe T et al (2004) Relationships between metal concentrations in great tit nestlings and their environment and food. Environ Pollut 131:373–380
Dauwe T et al (2005) Heavy-metal concentrations in female laying great tits (Parus major) and their clutches. Arch Environ Contam Toxicol 49:249–256
Dawson RD, Bidwell MT (2005) Dietary calcium limits size and growth of nestling tree swallows Tachycineta bicolor in a non-acidified landscape. J Avian Biol 36:127–134
Delmas F et al (1996) Expression of stress proteins in cultured human cells as a sensitive indicator of metal toxicity. Fresenius’ J Anal Chem 354:615–619
Deng HL et al (2007) Trace metal concentration in Great Tit (Parus major) and Greenfinch (Carduelis sinica) at the Western Mountains of Beijing, China. Environ Pollut 148:620–626
Edens FW et al (1976) Effect of dietary lead on reproductive performance in Japanese quail, Coturnix japonica. Toxicol Appl Pharmacol 38:307–314
Eeva T, Lehikoinen E (1996) Growth and mortality of nestling great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in a heavy metal pollution gradient. Oecologia 108:631–639
Eeva T, Lehikoinen E (2000) Improved breeding success in forest passerines after decreased emissions of heavy metals. Nature 403:851–852
Eeva T, Lehikoinen E, Rönkä M (1998) Air pollution fades the plumage of the Great Tit. Funct Ecol 12:607–612
Eeva T et al (2000) Biomarkers and fluctuating asymmetry as indicators of pollution-induced stress in two hole-nesting passerines. Funct Ecol 14:235–243
Eeva T, Lehikoinen E, Nikinmaa M (2003) Pollution-induced nutritional stress in birds: an experimental study of direct and indirect effects. Ecol Appl 13:1242–1249
Eeva T et al (2005a) Pollution related effects on immune function and stress in a free-living population of pied flycatcher Ficedula hypoleuca. J Avian Biol 36:405–412
Eeva T, Ryömä M, Riihimäki J (2005b) Pollution-related changes in diets of two insectivorous passerines. Oecologia 145:629–639
Eeva T et al (2008) Environmental pollution affects the plumage color of Great tit nestlings through carotenoid availability. EcoHealth 5:328–337
Eeva T, Ahola M, Lehikoinen E (2009a) Breeding performance of blue tits (Cyanistes caeruleus) and great tits (Parus major) in a heavy metal polluted area. Environ Pollut 157:3126–3131
Eeva T, Sillanpää S, Salminen J-P (2009b) The effects of diet quality and quantity on plumage colour and growth of Great tit nestlings: a food manipulation experiment along a pollution gradient. J Avian Biol 40:1–9
Eeva T et al (2012) Plasma carotenoid levels are not directly related to heavy metal exposure or reproductive success in three insectivorous passerines. Environ Toxicol Chem 31:1363–1369
Fair JM, Myers OB (2002) The ecological and physiological costs of lead shot and immunological challenge to developing western bluebirds. Ecotoxicology 11:199–208
Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552
Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432
Gil F, Pla A (2001) Biomarkers as biological indicators of xenobiotic exposure. J Appl Toxicol 21:245–255
Goyer RA (1997) Toxic and essential metal interactions. Annu Rev Nutr 17:37–50
Graveland J, van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314
Griffiths R et al (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Grue CE, O’Shea TJ, Hoffman DJ (1984) Lead concentrations and reproduction in highway-nesting barn swallows. Condor 86:383–389
Grue CE et al (1986) Lead concentrations and reproductive success in European starlings Sturnus vulgaris nesting within highway roadside verges. Environ Pollut Ser A 42:157–182
Guitart R et al (2009) Animal poisoning in Europe. Part 3: wildlife. Vet J 183:260–265
Hare L (1992) Aquatic insects and trace-metals—bioavailability, bioaccumulation, and toxicity. Crit Rev Toxicol 22:327–369
Harvey S et al (1984) Stress and adrenal function. J Exp Zool 232:633–645
Henny CJ et al (1994) Lead in hawks, falcons and owls downstream from a mining site on the Coeur D’Alene River, Idaho. Environ Monit Assess 29:267–288
Hoffman DJ et al (1985a) Survival, growth, and accumulation of ingested lead in nestling American kestrels (Falco sparverius). Arch Environ Contam Toxicol 14:89–94
Hoffman DJ et al (1985b) Biochemical and hematological effects of lead ingestion in nestling American kestrels (Falco sparverius). Comp Biochem Physiol B 80:431–439
Hogstad O (2001) Sexual difference in heavy metal contamination in the liver of tits Parus in winter. Ornis Fenn 78:39–43
Hutton M (1980) Metal contamination of feral pigeons Columba livia from the London area: part 2—biological effects of lead exposure. Environ Pollut, Ser A 22:281–293
Janssens E et al (2003a) Effects of heavy metal exposure on the condition and health of nestlings of the great tit (Parus major), a small songbird species. Environ Pollut 126:267–274
Janssens E et al (2003b) Breeding performance of great tits (Parus major) along a gradient of heavy metal pollution. Environ Toxicol Chem 22:1140–1145
Kendall RJ et al (1996) An ecological risk assessment of lead shot exposure in non-waterfowl avian species: upland game birds and raptors. Environ Toxicol Chem 15:4–20
Kiikkilä O (2003) Heavy-metal pollution and remediation of forest soil around the Harjavalta Cu–Ni smelter, in SW Finland. Silva Fenn 37:399–415
Koivula MJ et al (2011) Metal pollution indirectly increases oxidative stress in great tit (Parus major) nestlings. Environ Res 111:362–370
Laaksonen T et al (2004) Year- and sex-dependent effects of experimental brood sex ratio manipulation on fledging condition of Eurasian kestrels. J Anim Ecol 73:342–352
Lambrechts MM et al (2010) The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases. Acta Ornithol 45:1–26
Lawler EM, Duke GE, Redig PT (1991) Effect of sublethal lead exposure on gastric motility of red-tailed hawks. Arch Environ Contam Toxicol 21:78–83
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lobato E et al (2010) Arrival date and territorial behavior are associated with corticosterone metabolite levels in a migratory bird. J Ornithol 151:587–597
Loiseau C et al (2008) Condition-dependent effects of corticosterone on a carotenoid-based begging signal in house sparrows. Horm Behav 53:266–273
Lu H, Guizzetti M, Costa LG (2001) Inorganic lead stimulates DNA synthesis in human astrocytoma cells: role of protein kinase C alpha. J Neurochem 78:590–599
Lurie DI, Brooks DM, Gray LC (2006) The effect of lead on the avian auditory brainstem. Neurotoxicology 27:108–117
Mariño F, Winters C, Morgan AJ (1999) Heat shock protein (hsp60, hsp70, hsp90) expression in earthworms exposed to metal stressors in the field and laboratory. Pedobiologia 43:615–624
Martinez-de la Puente J et al (2011) Nest ectoparasites increase physiological stress in breeding birds: an experiment. Naturwissenschaften 98:99–106
Mateo R et al (1998) High prevalences of lead poisoning in wintering waterfowl in Spain. Arch Environ Contam Toxicol 35:342–347
Moreno J et al (2002) Heterophil/lymphocyte ratios and heat-shock protein levels are related to growth in nestling birds. Ecoscience 9:434–439
Morimoto RI, Tissiéres A, Georgopoulos C (1990) Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, Long Island
Möstl E et al (2002) Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 26:127–139
Nam DH, Lee DP (2006) Reproductive effects of heavy metal accumulation on breeding feral pigeons (Columba livia). Sci Total Environ 366:682–687
Nyholm NEI (1994) Heavy metal tissue levels, impact on breeding and nestling development in natural populations of pied flycatchers (Aves) in the pollution gradient from a smelter. In: Donker M, Eijsackers H, Heimback F (eds) Ecotoxicology of soil organisms. Lewis Publishers, Boca Raton, pp 373–382
Nyholm NEI et al (1995) Effects of environmental pollution on breeding populations of birds in southern Poland. Water Air Soil Pollut 85:829–834
Pain DJ (1989) Hematological parameters as predictors of blood lead and indicators of lead-poisoning in the black duck (Anas rubripes). Environ Pollut 60:67–81
Palme R et al (2013) Steroid extraction: get the best out of faecal samples. Wiener Tierarztliche Monatsschrift 100:238–246
Partali V et al (1985) Carotenoids in food chain studies—II. The food chain of Parus spp. monitored by carotenoid analysis. Comp Biochem Physiol 82:767–772
Peakall D (1992) Animal biomarkers as pollution indicators. Chapman & Hall
SAS (2008) SAS/STAT® 9.2 User’s Guide. SAS Institute Inc.
Scheuhammer AM (1987a) Erythrocyte delta-aminolevulinic-acid dehydratase in birds. 2. The effects of lead exposure in vivo. Toxicology 45:165–175
Scheuhammer AM (1987b) Erythrocyte α-aminolevulinic acid dehydratase in birds. I. The effects of lead and other metals in vitro. Toxicology 45:155–163
Scheuhammer AM (1987c) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295
Scheuhammer AM (1989) Monitoring Wild Bird Populations for Lead Exposure. Journal of Wildlife Management 53:759–765
Scheuhammer AM (1991) Effects of acidification on the availability of toxic metals and calcium to wild birds and mammals. Environ Pollut 71:329–375
Schilderman PAEL et al (1997) Possible relevance of pigeons as an indicator species for monitoring air pollution. Environ Health Perspect 105:322–330
Sillanpää S et al (2008) Carotenoids in a food chain along a pollution gradient. Sci Total Environ 406:247–255
Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037
Stöwe M et al (2008) Corticosterone excretion patterns and affiliative behavior over development in ravens (Corvus corax). Horm Behav 53:208–216
Stöwe M et al (2010) Selection for fast and slow exploration affects baseline and stress-induced corticosterone excretion in Great tit nestlings, Parus major. Horm Behav 58:864–871
Tilgar V et al (2004) Calcium availability affects bone growth in nestlings of free-living great tits (Parus major), as detected by plasma alkaline phosphatase. J Zool 263:269–274
Tomás G, Martínez J, Merino S (2004) Collection and analysis of blood samples to detect stress proteins in wild birds. J Field Ornithol 75:281–287
van Balen JH (1973) A comparative study of the breeding ecology of the great tit Parus major in different habitats. Ardea 61:1–93
Vanparys C et al (2008) Metallothioneins (MTs) and delta-aminolevulinic acid dehydratase (ALAd) as biomarkers of metal pollution in great tits (Parus major) along a pollution gradient. Sci Total Environ 401:184–193
Youssef SAH et al (1996) Effect of subclinical lead toxicity on the immune response of chickens to Newcastle disease virus vaccine. Res Vet Sci 60:13–16
Zhong ZM et al (2010) Chronic prenatal lead exposure impairs long-term memory in day old chicks. Neurosci Lett 476:23–26
Acknowledgments
We thank Salla Koskinen, Päivi Kotitalo, Tarja Pajari, Marjo Aikko, Orsolyia Palfi and Jorma Nurmi for their efforts in helping us with field work. Orsolyia Palfi is acknowledged for the ALAd analyses and Samy El Makarem for help with the CORT measurements. Tuija Koivisto made the color measurements. Meri Lindquist is acknowledged for molecular sexing of birds. Paul Ek and Sten Lindholm (Åbo Akademi) are acknowledged for the heavy metal analyses. Our study was financed by KONE foundation (SR: project 28-1274) and Academy of Finland (TE: project 265859).
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Eeva, T., Rainio, M., Berglund, Å. et al. Experimental manipulation of dietary lead levels in great tit nestlings: limited effects on growth, physiology and survival. Ecotoxicology 23, 914–928 (2014). https://doi.org/10.1007/s10646-014-1235-5
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DOI: https://doi.org/10.1007/s10646-014-1235-5